Colonization in North American Arid Lands: The Journey of Agarito (Berberis trifoliolata) Revealed by Multilocus Molecular Data and Packrat Midden Fossil Remains

Abstract

Here we conduct research to understand the evolutionary history of a shrubby species known as Agarito (Berberis trifoliolata), an endemic species to the Chihuahuan Desert. We identify genetic signatures based on plastid DNA and AFLP markers and perform niche modelling and spatial connectivity analyses as well as niche modelling based on records in packrats to elucidate whether orogenic events such as mountain range uplift in the Miocene or the contraction/expansion dynamics of vegetation in response to climate oscillations in the Pliocene/Pleistocene had an effect on evolutionary processes in Agarito. Our results of current niche modelling and palaeomodelling showed that the area currently occupied by Berberis trifoliolata is substantially larger than it was during the Last Interglacial period and the Last Glacial Maximum. Agarito was probably confined to small areas in the Northeastern and gradually expanded its distribution just after the Last Glacial Maximum when the weather in the Chihuahuan Desert and adjacent regions became progressively warmer and drier. The most contracted range was predicted for the Interglacial period. Populations remained in stable areas during the Last Glacial Maximum and expanded at the beginning of the Holocene. Most genetic variation occured in populations from the Sierra Madre Oriental. Two groups of haplotypes were identified: the Mexican Plateau populations and certain Northeastern populations. Haplogroups were spatially connected during the Last Glacial Maximum and separated during interglacial periods. The most important prediction of packrat middens palaeomodelling lies in the Mexican Plateau, a finding congruent with current and past niche modelling predictions for agarito and genetic results. Our results corroborate that these climate changes in the Pliocene/Pleistocene affected the evolutionary history of agarito. The journey of agarito in the Chihuahuan Desert has been dynamic, expanding and contracting its distribution range and currently occupying the largest area in its history.

Fig 1. Populations of Berberis trifoliolata studied and their haplotypes.

Pie charts represent the haplotypes found in each sampling locality. Size of sections is proportional to the number of individuals with that haplotype. The size of circles in the haplotype network is proportional to the frequency of each haplotype. Population names are given in Table 1. Red line shows the division between the Mexican Plateau and the Northeastern populations.

Fig 2

A) Flowers and habit of Berberis trifoliolata. B) Bayesian chronogram showing the time of divergence Agarito haplotypes. Colours of the squares correspond to those of Fig 1. The 95% credibility intervals are shown by purple bars.

Fig 3. Results of the Bayesian skyline plots (left) and Mismatch distribution (right).

A and B correspond to Northeastern populations and C and D corresponds to Mexican Plateau populations. Solid lines in A and C are estimates of means.

Fig 4. Bayesian assignment analysis showing the spatial genetic structure of Berberis trifoliolata populations.

A) Bar plots depicting the results of two rounds of hierarchical STRUCTURE analyses A1) First level of analysis showing K = 2 fit the genetic groups the best A2) Second level of analysis showing substructure. White vertical lines separate sets of individuals of different populations. B) Map showing the populations sampled and the proportion of the genome as determined by second-level STRUCTURE analysis. The codes indicate sampling localities given in Table 1.

Fig 5. Ecological niche modelling for Berberis trifoliolata.

Black dots indicate sampled localities. A) Current potential distribution. B) Predicted distribution during the Interglacial period. C) Predicted distribution during the Last Glacial Maximum (CCSM model). D) Predicted distribution during the Last Glacial Maximum (MIROC model). Blue dots indicate records without coordinates. Green stars indicate packrats middens containing Quaternary fossil remains of agarito. Color range from pink to light red to red colors indicates low, medium and high probability, respectively.

Fig 6. Connectivity maps among populations for Berberis trifoliolata.

Colder (blue) colours indicate areas with stronger connectivity; areas where connectivity is tenuous are shown in warmer colours. A) Present; B) Last Glacial Maximum (CCSM model); C) Last Interglacial. The red line delimits the division between the Mexican Plateau and Northeastern groups of populations.